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. 2023 Nov 2;15(2):210–237. doi: 10.1080/21501203.2023.2265667

Four new species of Russula from the Xizang Autonomous Region and other provinces of China

Shi-Hui Wang a,b,#, Guo-Jie Li c,#, Dorji Phurbu d, Mao-Qiang He a, Ming-Zhe Zhang a,e, Xin-Yu Zhu a, Jia-Xin Li a,e, Rui-Lin Zhao a,e,, Bin Cao a,e,
PMCID: PMC11132434  PMID: 38813475

ABSTRACT

Russula is the largest genus in the Russulales and is widespread throughout the world. Almost all Russula species are known to be ectomycorrhizal with high ecological and edible values, and some are lethal poisonous. In this study, four new species belonging to the subgenus Russula crown clade are identified based on morphological and phylogenetic evidence from the Xizang Autonomous Region and other provinces of China. Morphologically, Russula paragraveolens (sect. Polychromae, subsect. Xerampelinae) is mainly characterised by a cherry red to blood red pileus centre, a reddish orange pileus margin; R. pseudograveolens (sect. Polychromae, subsect. Xerampelinae) is characterised by a violet brown to brownish red pileus centre, a pale red to pastel red pileus margin and short basidia; R. shigatseensis (sect. Flavisiccantes, subsect. Lepidinae) is characterised by a brownish orange to madder red pileus centre, pinkish red pileus margin, and having lateral branches or branches of hyphal terminations in pileipellis; R. yadongensis (sect. Tenellae, subsect. Laricinae) is characterised by a dark purplish red pileus centre with brownish purple tints and having isolated to clustered spines of spore ornamentations. Their distinct taxonomic status is confirmed by the positions of the four new species in both the ITS and 4-locus (nucLSU, mtSSU, rpb2, tef1) phylogenetic trees.

KEYWORDS: Agaricomycetes, morphology, phylogeny, Russulales, taxonomy

1. Introduction

Russula Pers. belongs to the Basidiomycota, Agaricomycetes, Russulales, Russulaceae, and is the type genus of Russulaceae (Kirk et al. 2008; He et al. 2019). Russula species are widespread throughout the world, from the tundra of Greenland in the north to the broad-leaved forest of New Zealand in the south (Looney et al. 2015). They form ectomycorrhizae with gymnosperms, such as Abies, Larix, Picea, Pinus, and Pseudotsuga, and angiosperms, such as Fabaceae, Fagales, Malpighiales, and Myrtaceae. They increase plant resistance, promote root growth and nutrient uptake, and closely correspond to the plant communities (Looney et al. 2018; Sarwar et al. 2020). Many species of Russula are important wild edible mushrooms, rich in nutritional elements, with anti-tumour, antioxidant, cholesterol-lowering, blood lipid-lowering, and blood sugar-lowering effects, such as Russula cyanoxantha (Schaeff.) Fr. and R. griseocarnosa X.H. Wang, Zhu L. Yang & Knudsen (Chen and Zhang 2010; Kaewnarin et al. 2016; Khatua et al. 2021; Liu et al. 2023). However, there are also toxic species such as R. emetica (Schaeff.) Pers. and R. senecis S. Imai, which often cause gastroenteritis-type poisoning when accidentally consumed. Russula subnigricans Hongo is a highly toxic species that has caused many deaths in food poisoning incidents (Chen et al. 2014; Cho and Han 2016; Matsuura et al. 2016).

In recent years, due to the rapid development of molecular biology techniques, the taxonomic research of Russula has been promoted. Phylogenetic relationships of infrageneric taxa have been more objectively elucidated. The latest classification system shows that the genus comprises eight subgenera, Archaeae Buyck & V. Hofst., Brevipedum Buyck & V. Hofst., Compactae (Fr.) Bon, Crassotunicatae Buyck & V. Hofst., Glutinosae Buyck & X.H. Wang, Heterophyllidiae Romagn., Malodorae Buyck & V. Hofst., Russula Buyck & V. Hofst (Looney et al. 2015; Buyck et al. 2018, 2020; Adamčík et al. 2019). Among them, subg. Russula consists of two major clades: The Russula core clade and the Russula crown clade. Since 2006, at least 68 new species have been published for the crown clade of subg. Russula, 48 of which are from Asia, and 23 new species have been described for this clade from China, demonstrating the extraordinary species richness of this clade of the Russula crown clade (Li et al. 2012, 2013a, 2013b, 2015, 2016; Jiang et al. 2018; Li et al. 2018a, 2018b, 2021; Caboň et al. 2019; Song et al. 2021; Li 2022; Zhou et al. 2022). Members of Russula crown clade mostly have unchanging, yellowing, browning, reddening, greying, or blackening of context when bruised, sometimes with distinct disagreeable to agreeable smell, mild to strongly acrid tasted context, white to yellow spore print (Buyck et al. 2018). Four new species of this clade were also identified in our macrofungal diversity survey, and these four new species were elucidated by morphological and phylogenetic analyses in this study.

2. Materials and methods

2.1. Morphological study

During collection, the macro-morphological characteristics of the specimens and the habitat were photographed with a camera (Canon EOS 80D), and fresh specimens were wrapped in tin foil in order to avoid mixing or crushing. After recording the macro-morphological characteristics in the field, the fresh specimens were dehydrated in a drying oven at 55 °C for 12 h in the laboratory. The dried specimens were deposited in the Mycological Herbarium, Institute of Microbiology, Chinese Academy of Sciences (HMAS). The description followed the criteria for Russula morphology observation (Adamčík et al. 2019). The colour designation refers to HTML Color Codes (https://htmlcolorcodes.com).

Specimens were rehydrated with 5% KOH solution. Observation of spores was made in Melzer’s reagent. The morphology of hymenial cystidia and pileocystidia were stained with 1% aqueous Congo red solution (Heilmann-Clausen et al. 2000). Tissues of the pileus were also examined in Cresyl Blue solution to verify the presence of a metachromatic reaction (Buyck 1989). Carbolfuchsin was used to observe incrustations on primordial hyphae (Singer 1968). Sulfovanillin was used to observe the colouring of cystidia contents (Caboň et al. 2017).

2.2. DNA extraction, PCR and sequencing

DNA was extracted from 5 to 20 mg tissue of dried specimen with the Broad-spectrum Plant Rapid Genomic DNA Kit (Biomed, Beijing) following the manufacturer’s instructions.

In this study, five loci were amplified and sequenced: ITS was amplified using primer pair ITS1-F/ITS4 (White et al. 1990); ribosomal nuclear large subunit (nucLSU) was amplified by LROR/LR5 (Moncalvo et al. 2000); ribosomal mitochondrial small subunit (mtSSU) was amplified by MS1/MS2 (White et al. 1990); second largest subunit of the RNA polymerase II (rpb2) was amplified by RPB2-6F/RPB2–7.1R (Matheny 2005); translation elongation factor 1-alpha (tef1) was amplified by EF1-983F/EF1-1567R (Rehner and Buckley 2005). The amplified PCR products were detected by electrophoresis and sent to BGI Genomics Co., Ltd. (Beijing) for purification and sequencing.

2.3. Molecular phylogenetic study

Newly generated and reference sequences obtained from GenBank are listed in Tables 1 and 2. The sequences were aligned in AliView v1.19 and manually adjusted to eliminate poorly aligned or ambiguous regions. The six partitions were assembled in PhyloSuite v1.2.2 (Zhang et al. 2020), in the order of six loci (nucLSU, mtSSU, rpb2 exons, rpb2 introns, tef1 exons, tef1 introns). The final alignments have been deposited in TreeBASE (study no. 30337, 30338).

Table 1.

Sequences used in phylogenetic analysis based on ITS.

Taxon Voucher specimen Location ITS accession number
Gymnomyces abietis - USA AY239347
Gymnomyces abietis - USA AY239348
Gymnomyces californicus - USA AY239312
Gymnomyces californicus - USA AY239308
Gymnomyces foetens - USA AY239316
Gymnomyces monticola - USA AY239313
Gymnomyces monticola - USA AY239314
Gymnomyces setigerus - USA AY239317
Gymnomyces subalpinus - USA AY239309
Gymnomyces subalpinus - USA AY239311
Macowanites vinaceodorus - Spain AJ438034
Macowanites vinaceodorus 46374 (AH) Spain MK105695
Russula abbottabadensis FH00304589 (holotype) Pakistan MG386704
Russula abietiphila HCCN14799 (type) South Korea MN130060
Russula abietiphila HCCN18498 South Korea MN130061
Russula adwanitekae AG 16-1430 (type) India MN263242
Russula adwanitekae AG 16-1435 India MN263243
Russula amethystina LAH35058 (holotype) Pakistan KT953613
Russula amoenipes 309IS77 USA AY061656
Russula aurantioflammans r3245 Slovakia KU928167
Russula brunneovinacea RITF 2242 (holotype) China KY114148
Russula brunneoviolacea MC01-507 Denmark AM113956
Russula brunneoviolacea PRM 922,557 Canada MG687327
Russula buyckii CUHAM277 (holotype) India KT962833
Russula cessans CR19 Canada KP406550
Russula changbaiensis HMAS262369 (holotype) China KC412162
Russula claroflava 224IS76 USA AY061665
Russula claroflava FH12212 USA KT933997
Russula clavatohyphata CAL1756 (holotype) India MG934209
Russula clavipes SAV:F-1327 Slovakia KU205292
Russula coronaspora GDGM79711 (holotype) China MN275689
Russula coronaspora GDGM79712 China MN275690
Russula cremeirosea BPL289 USA KT933983
Russula cremeoavellanea SAV F-2125 Slovakia KY582695
Russula cuprea FH12250 USA KT934010
Russula curtipes 1123IS77 USA AY061668
Russula curtipes FH12206 USA KT933995
Russula decolorans - Germany AF418637
Russula decolorans FH12196 USA KT933992
Russula dhakuriana CUHAM343 India MK414576
Russula emeticicolor FH12253 USA KT934011
Russula faginea SAV F-1337 France KU205289
Russula faginea SAV F-997 Slovakia KU205286
Russula favrei SAV F-1333 Finland KU205311
Russula favrei UPS UE06.09.2003-9 Sweden KU205272
Russula firmula AT2004142 Sweden DQ422017
Russula flavobrunnescens TLXM (AK5024) (type) Mexico MN130082
Russula fontqueri FH12223 USA KT934003
Russula gnathangensis CAL1733 (holotype) India MK253441
Russula graveolens SAV F-1342 Slovakia KU205302
Russula graveolens SAV:F-1338 Belgium KU205306
Russula griseocarnosa KUN F51839 (holotype) China EF627042
Russula griseocarnosa - China EF627043
Russula guangxiensis HMAS267867 (holotype) China KT286852
Russula hakkae HMAS267765 (holotype) China KT286848
Russula heilongjiangensis HMAS255142 (holotype) China MG719932
Russula hookeri CUHAM275 (holotype) India KP713777
Russula integra FH12172 USA KT933984
Russula jilinensis HMAS194253 (holotype) China GU966632
Russula katarinae BB03.159 (PC) (holotype) USA KP966377
Russula katarinae BB03.159 (holotype) USA NR153255
Russula kewzingensis CAL1636 (holotype) India MG674302
Russula khinganensis HMAS278895 (holotype) China MG719928
Russula laeta SAV F-3949 Slovakia KY582708
Russula laricina BB 08.681 Italy JN944008
Russula laricina E Watling 25556 Europe AY061685
Russula lepida - Germany AF418641
Russula madrensis TLXM (AK3422) (type) Mexico MN130093
Russula magica GENT (FH12-061) (type) Thailand MN130096
Russula messapica var. messapica ALV1991 Spain MK105669
Russula messapica var. messapicoides JL1493 Spain MK105674
Russula minor GDGM79686 (holotype) China MN275666
Russula minor GDGM79687 China MN275665
Russula nauseosa F30315 Canada KJ748441
Russula nauseosa F30317 Canada KJ748443
Russula nuoljae HMJAU37320 China KY357333
Russula nuoljae SAV:F-3092 Norway KU205350
Russula nympharum FH11121505 (holotype) Spain KU928157
Russula odorata BB 07.186 Slovakia JN944010
Russula olivaceohimalayensis CAL 1659 (AG 17-1447) (type) India MN130097
Russula olivaceohimalayensis CAL 1664 (AG 15-910) India MN130098
Russula paragraveolens HMAS281158 (holotype) China OQ871504
Russula paragraveolens HMAS279574 China OQ871506
Russula paragraveolens HMAS279575 China OQ871505
Russula pascua IB:1998/0124 Germany KU205314
Russula peckii BPL270 USA KT933970
Russula pseudograveolens HMAS279577 China OQ871507
Russula pseudograveolens HMAS279579 China OQ871508
Russula pseudograveolens HMAS287385 China OQ871497
Russula pseudograveolens HMAS287384 (holotype) China OQ871496
Russula pseudotsugarum UBC:F33077 Canada MF908478
Russula pseudotsugarum UWBM:WTU-F-038562 (type) USA KX813578
Russula puellaris nl1372 (TUB) Germany AF418628
Russula puellula SAVF 3107 Slovakia KY582704
Russula purpureoverrucosa GDGM32902 (holotype) China MG214692
Russula purpureozonate KD 18-003 (type) India MN267570
Russula purpureozonate KD 18-15 India MN269951
Russula pusilla BPL267 USA KT933968
Russula rosea BB 07.780 France JN944003
Russula rubra SAV F-914 Slovakia KY582723
Russula rugulosa BPL654 USA KY848516
Russula rutila SAV F-1504 Slovakia KY582687
Russula sancti-pauli PC (BB 06.494) (type) Mexico MN130101
Russula sancti-pauli PC (BB 06.499) Mexico MN130102
Russula sapinea PA38 Latvia KR019818
Russula seperina GENT (Verbeken 2000-135) Italy MN130109
Russula seperina SAV F-3156 (type) Slovakia MN130108
Russula shigatseensis HMAS287390 China OQ871502
Russula shigatseensis HMAS287389 (holotype) China OQ871501
Russula shigatseensis HMAS287391 China OQ871503
Russula sichuanensis HKAS 53885 China JX391968
Russula sichuanensis HKAS53792 (holotype) China JX391969
Russula sichuanensis HMAS 255316 China MG786566
Russula solaris BB 07.282 Slovakia JN944007
Russula sp. FLAS-F-61146 USA MH211767
Russula sp. FLAS-F-61609 USA MH211995
Russula sp. HMAS:260700 China KX441055
Russula sp. JLF6993 USA MN263039
Russula sp. LM1553 UK KM576511
Russula sp. S.D. Russell 439 USA MK397035
Russula sp. SR48-10MX Mexico KT697966
Russula sp. F30324 Canada KJ748450
Russula sp. S.D. Russell 7799 USA MK532803
Russula subrutilans RITF1874 (holotype) China KJ868237
Russula subsulphurea F18743 Europe KF810135
Russula subsulphurea TENN:F18743 USA NR153231
Russula subtilis SAV F-3805 (type) USA KY509504
Russula subtilis TENN-F-067624 (BPL666) (type) USA KY509511
Russula tengii HMAS262728 (holotype) China MG386708
Russula tinctipes SAVF-2494 Slovakia KY582698
Russula uttarakhandia CAL 1537 (holotype) India KY873997
Russula velenovskyi 526IS77 USA AY061721
Russula versatilis PRM 922558 Czech Republic MG687329
Russula versicolor BB 07.288 Slovakia JN944009
Russula veternosa SAV F-2588 Slovakia KY582699
Russula vidalii JC100508BT01, JMV800688 (BCN) Spain MK105693
Russula vidalii JMV20160517-1 (BCN) Spain MK105694
Russula vinosa nl1386 Germany AF418638
Russula vinosa SAV F-20024 Slovakia KY582692
Russula vinosobrunneola HMAS 278885 China MG719925
Russula vinosobrunneola HMAS281138 (holotype) China MG719927
Russula violaceoincarnata O73136 Netherland GU234047
Russula xerampelina DG05-28 UK JQ888204
Russula xerampelina UPS:UE14.09.2004-3 Sweden KU205279
Russula yadongensis HMAS287387 China OQ871499
Russula yadongensis HMAS287386 (holotype) China OQ871498
Russula yadongensis HMAS287388 China OQ871500
Russula zelleri NYGB-761009 (type) USA KX812833
Russula zelleri OSC 5610 USA MK169364
Russula zvarae BB 08.639 Italy JN944004
Outgroup      
Russula emetica lw81 (TUB) Germany AF418619
Russula emetica UE05.10.2003-11 Sweden DQ421997

Newly generated sequences are shown in bold.

Table 2.

Sequences used in phylogenetic analysis based on 4-locus data.

Taxon Voucher specimen Location nucLSU mtSSU rpb2 tef1
R. aff. fucosa 27/BB 06.596 Canada KU237457 KU237301 KU237743 KU237892
R. aff. subdensifolia 552/BB 07.158 USA KU237544 KU237390 KU237830 KU237974
R. aff. turci 433/BB 07.325 Slovakia KU237497 KU237342 KU237783 KU237927
R. aff. viscidula 73/BB 06.049 Madagascar KU237469 KU237313 KU237755
R. aff. xerampelina 592/DM fl07-14 USA KU237576 KU237424 KU237862 KU238004
R. amara 532/BB 07.782 France KU237524 KU237370 KU237810 KU237954
R. amethystina 529/BB 07.314 Slovakia KU237521 KU237367 KU237807 KU237951
R. aurata 547/BB 07.211 Slovakia KU237539 KU237385 KU237825 KU237969
R. azurea 537/BB 08.668 Italy KU237529 KU237375 KU237815 KU237959
R. badia 587/BB 07.324 Slovakia KU237571 KU237419 KU237857 KU237999
R. burlinghamiae 548/BB 05.108 USA KU237540 KU237386 KU237826 KU237970
R. carminipes 531/BB 07.192 Slovakia KU237523 KU237369 KU237809 KU237953
R. carpini 551/BB 07.262 Slovakia KU237543 KU237389 KU237829 KU237973
R. cf. aurantioflammans 241/BB 06.603 Canada KU237488 KU237332 KU237774 KU237917
R. cf. brunneoviolacea 524/BB 06.606 Canada KU237516 KU237362 KU237802 KU237946
R. cf. decipiens 231/BB 06.521 Mexico KU237482 KU237326 KU237768 KU237911
R. cf. katarinae 30/BB 06.617 Canada KU237460 KU237304 KU237746 KU237895
R. cf. odorata 525/BB 07.219 Slovakia KU237517 KU237363 KU237803 KU237947
R. cf. olivobrunnea 240/BB 06.505 Mexico KU237487 KU237331 KU237773 KU237916
R. cf. sejuncta 557/BB 08.143 Madagascar KU237547 KU237393 KU237833
R. cf. sesenagula 84/BB 06.129 Madagascar KU237473 KU237317 KU237759 KU237904
R. cf. vinosobrunea 533/BB 07.231 Slovakia KU237525 KU237371 KU237811 KU237955
R. citrinolutea sp. ined. 29/BB 06.611 Canada KU237459 KU237303 KU237745 KU237894
R. corallina 229/BB 06.324 USA KU237481 KU237325 KU237767 KU237910
R. cuprea 565/BB 07.233 Slovakia KU237555 KU237401 KU237841 KU237984
R. decipiens 585/BB 07.178 Slovakia KU237569 KU237417 KU237855 KU237997
R. decolorans 549/BB 07.322 Slovakia KU237541 KU237387 KU237827 KU237971
R. discopus 48/BB 06.027 Madagascar KU237467 KU237311 KU237753 KU237900
R. echinospermatinae sp. ined. 736/BB 09.173 New Caledonia KU237589 KU237437 KU237874 KU238016
R. flavisiccans 236/BB 06.336 Mexico KU237485 KU237329 KU237771 KU237914
R. gigasperma 438/BB 07.280 Slovakia KU237501 KU237346 KU237787 KU237931
R. globispora 436/BB 07.243 Slovakia KU237499 KU237344 KU237785 KU237929
R. heinemannianus 594/CS s.n. Zimbabwe KU237577 KU237425 KU237863 KU238005
R. integra 518/BB 07.198 Slovakia KU237513 KU237359 KU237799 KU237943
R. laeta 519/BB 07.267 Slovakia KU237514 KU237360 KU237800 KU237944
R. laricina 575/BB 08.681 Italy KU237560 KU237408 KU237846 KU237991
R. lepida 437/BB 07.189 Slovakia KU237500 KU237345 KU237786 KU237930
R. lilacea 435/BB 07.213 Slovakia KU237498 KU237343 KU237784 KU237928
R. melliolens 554/BB 07.194 Slovakia KU237545 KU237391 KU237831 KU237975
R. musaecolor sp. ined. 558/BB 08.063 Madagascar KU237548 KU237394 KU237834 KU237977
R. nauseosa 588/BB 07.285 Slovakia KU237572 KU237420 KU237858 KU238000
R. nothofagineae sp. ined. 723/BB 09.044 New Caledonia KU237583 KU237431 KU238010
R. nothofagineae sp. ined. 725/BB 09.068 New Caledonia KU237584 KU237432 KU237869 KU238011
R. nothofagineae sp. ined. 726/BB 09.069 New Caledonia KU237585 KU237433 KU237870 KU238012
R. nothofagineae sp. ined. 732/BB 09.124 New Caledonia KU237586 KU237434 KU237871 KU238013
R. nothofagineae sp. ined. 733/BB 09.125 New Caledonia KU237587 KU237435 KU237872 KU238014
R. obscurosordida sp. ined. 591/BB 06.564 Canada KU237575 KU237423 KU237861 KU238003
R. odorata 526/BB 07.186 Slovakia KU237518 KU237364 KU237804 KU237948
R. olivacea 426/BB 07.223 Slovakia KU237492 KU237336 KU237778 KU237921
R. olivascens 530/BB 08.663 Italia KU237522 KU237368 KU237808 KU237952
R. paludosa 442/BB 07.330 Slovakia KU237505 KU237350 KU237791 KU237935
R. paragraveolens HMAS281158 China OQ875223 OQ878262 OQ933792 OQ948122
R. paragraveolens HMAS279574 China OQ875224 OQ878263 OQ933793 OQ948123
R. pelargonia 586/BB 07.169 Slovakia KU237570 KU237418 KU237856 KU237998
R. pseudograveolens HMAS279577 China OQ875227 OQ878266 OQ933794 OQ948121
R. pseudograveolens HMAS287385 China OQ875226 OQ878265 OQ933796 OQ948120
R. pseudograveolens HMAS287384 China OQ875225 OQ878264 OQ933795 OQ948119
R. puellaris 523/BB 07.311 Slovakia KU237515 KU237361 KU237801 KU237945
R. romellii 427/BB 07.202 Slovakia KU237493 KU237337 KU237779 KU237922
R. rosea 430/BB 07.780 France KU237496 KU237340 KU237782 KU237925
R. roseinae sp. ined. 735/BB 09.172 New Caledonia KU237588 KU237436 KU237873 KU238015
R. shigatseensis HMAS287390 China OQ875231 OQ878270 OQ933788 OQ948115
R. shigatseensis HMAS287389 China OQ875230 OQ878269 OQ933787 OQ948114
R. shigatseensis HMAS387391 China OQ875232 OQ878271 OQ933789 OQ948116
R. sichuanensis HMAS255316 China MG786572 MG792323 MG812160
R. sichuanensis HMAS268888 China KX441372 KX441619 MF893457
R. solaris 559/BB 07.282 Slovakia KU237549 KU237395 KU237835 KU237978
R. subtilis 536/BB 05.107 USA KU237528 KU237374 KU237814 KU237958
R. tlaxcalae 33/BB 06.542 Mexico KU237463 KU237307 KU237749 KU237897
R. turci 528/BB 07.328 Slovakia KU237520 KU237366 KU237806 KU237950
R. versicolor 589/BB 07.288 Slovakia KU237573 KU237421 KU237859 KU238001
R. vinosobrunneola HMAS278885 China MG786570 MG792321 MG812158
R. vinosobrunneola HMAS281138 China MG786569 MG792320 MG812157
R. vinosobrunneola HMAS278896 China MG786567 MG792318 MG812155
R. vinosobrunneola HMAS278960 China MG786568 MG792319 MG812156
R. yadongensis HMAS287386 China OQ875228 OQ878267 OQ933790 OQ948117
R. yadongensis HMAS287388 China OQ875229 OQ878268 OQ933791 OQ948118
R. zvarae 538/BB 08.639 Italy KU237530 KU237376 KU237816 KU237960
Outgroup            
R. raoultii 561/BB 08.674 Italy KU237551 KU237397 KU237837 KU237980
R. viscida 425/BB 07.298 Slovakia KU237491 KU237335 KU237777 KU237920

Newly generated sequences are shown in bold.

The ITS-based phylogenetic analysis consisted of 152 sequences representing 109 species, with R. emetica as the outgroup. A total of 80 concatenated sequences representing 66 species were used for multigene phylogenetic analyses, with R. raoultii Quél. and R. viscida Kudřna as the outgroups. The ITS and concatenated sequences were analysed using RAXMLGUI 1.3.1 (Silvestro and Michalak 2012) with the GTRGAMMAI model and 1,000 rapid bootstrap (BS) replicates. The best-fit model for ITS was selected using ModelFinder in PhyloSuite v1.2.2 (Kalyaanamoorthy et al. 2017). The best partitioning scheme and evolutionary models for six predefined partitions were selected using PartitionFinder2 in PhyloSuite v1.2.2 (Lanfear et al. 2017). Bayesian inference (BI) analyses was performed using MrBayes 3.2.6 (Ronquist et al. 2012) under the best model. Four Markov chains were run for 2 million generations, stopping when the average standard deviation of split frequencies fell below 0.01. Trees were sampled every 100th generation. The initial 25% of sampled data were discarded as burn-in.

The resulting file after tree construction was used to view the phylogenetic tree using FigTree 1.4.3 (Andrew 2016). Bootstrap Support (BS) ≥70% considered significantly supported. Bayesian Posterior Probability (PP) ≥95% was regarded as significant.

3. Results

3.1. Phylogeny

The best evolutionary model was selected using ModelFinder, with the BIC criterion: HKY+F+I+G4 for ITS. The best partitioning scheme and evolutionary models for six predefined partitions were selected using PartitionFinder2 (Lanfear et al. 2017), with greedy algorithm and AICc criterion: GTR+I+G for nucLSU, GTR+I+G for mtSSU, SYM+I+G for rpb2 exons, HKY+G for rpb2 introns, SYM+I+G for tef1 exons, GTR+I+G for tef1 introns.

Maximum likelihood and Bayesian analyses were performed on the ITS and 4-locus data sets, and both maximum likelihood and Bayesian analyses yielded the same topology. The four proposed new species, R. paragraveolens, R. pseudograveolens, R. shigatseensis, and R. yadongensis, are all nested in the Russula crown clade in both ITS and 4-locus (nucLSU-mtSSU-rpb2-tef1) trees, and are clearly separated from known species (Figures 1 and 2).

Figure 1.

Figure 1.

(Continued).

Figure 2.

Figure 2.

(Continued).

Figure 1.

Figure 1.

Maximum likelihood tree of subgen. Russula crown clade based on ITS sequences, bootstrap values higher than 70% were displayed around nodes. Accession numbers of the four species are shown in red. “T” refers to a type specimen.

Figure 2.

Figure 2.

Maximum likelihood tree of subgen. Russula crown clade based on 4-locus (nucLSU-mtSSU-rpb2-tef1) combined sequences, bootstrap values higher than 70% were displayed around nodes. Collections of the two novel species are shown in red. “T” refers to a type specimen.

3.2. Taxonomy

Russula paragraveolens S.H. Wang, G.J. Li, R.L. Zhao & B. Cao, sp. nov., Figures 3a, 4a, 4b, 5, 6, 13a

Figure 3.

Figure 3.

Basidiomata in the field. (a) Russula paragraveolens (HMAS281158, holotype). (b) R. pseudograveolens (HMAS287384, holotype). (c–d) R. pseudograveolens (HMAS279577). (e–f) R. pseudograveolens (HMAS279579). (g–h) R. yadongensis (HMAS287387). (i) R. yadongensis (HMAS287386, holotype). (j) R. yadongensis (HMAS287388). (k–l) R. shigatseensis (HMAS287390). (m) R. shigatseensis (HMAS287389, holotype). (n–o) R. shigatseensis (HMAS287391).

Figure 4.

Figure 4.

Basidiospores under scanning electron microscope. (a–b) Russula paragraveolens (HMAS281158, holotype). (c–d) R. pseudograveolens (HMAS287384, holotype). (e–f) R. yadongensis (HMAS287386, holotype). (g–h) R. shigatseensis (HMAS287389, holotype).

Figure 5.

Figure 5.

Russula paragraveolens (HMAS281158, holotype), hymenium. (a) Basidia. (b) Basidiola. (c) Marginal cells on the lamella edges. (d) Hymenial cystidia near the lamella sides. (e) Hymenial cystidia on the lamella edges. Cystidia with contents as observed in Congo red. Scale bar = 10 μm.

Figure 6.

Figure 6.

Russula paragraveolens (HMAS281158, holotype), pileipellis. (a) Pileocystidia near the pileus centre. (b) Hyphal terminations near the pileus centre. (c) Pileocystidia near the pileus margin. (d) Hyphal terminations near the pileus margin. Cystidial contents as observed in Congo red. Scale bar = 10 μm.

Figure 13.

Figure 13.

Spore drawings showing ornamentation in Melzer reagent. (a) Russula paragraveolens (HMAS281158, holotype). (b) R. pseudograveolens (HMAS287384, holotype). (c) R. shigatseensis (HMAS287389, holotype). (d) R. yadongensis (HMAS287386, holotype). Scale bar = 2 μm.

Fungal Names: FN571273.

Typification CHINA. Jilin Province, Yanbian Korean Autonomous Prefecture, Wangqing County, Mantianxing National Forest Park, N 43°18′ E 129°45′, 381 m asl, 22 July 2016, Ming-Zhe Zhang, Xu-Ming Bai, Rong-Chun Dai, Guo-Jie Li, ZRL20160546 (holotype HMAS281158). GenBank: OQ871504 (ITS), OQ875223 (nucLSU), OQ878262 (mtSSU), OQ933792 (rpb2), OQ948122 (tef1).

Etymology Named after its similarity to the species R. graveolens Romell.

Diagnosis Pileus medium-sized, with bright red tinge; lamellae dense, with yellowish white to pale yellow colour; stipe 25–40 × 10–17 mm, cylindrical and slightly thick near the base; spores (5.0–)5.5–5.9–6.3(−6.6) × (4.0–)4.6–5.0–5.4(−5.6) μm, broadly ellipsoid, large, with isolated or occasionally fused, prominent spines; basidia (31–)31–36–41(−50) × (10–)10–11–12(−14) μm, clavate; hymenial cystidia (42–)53–59–64(−71) × (8–)9–10(−11) μm, mainly clavate or fusiform, apically acute; hyphal terminations near the pileus margin occasionally narrow, thin-walled, terminal cells mainly cylindrical, apically obtuse or slightly constricted.

Pileus medium-sized, 40–70 mm diam., applanate with depressed centre; margin crenulate; cuticle smooth and shiny, peeling to 3/4 of the radius, bright red tinge (#AE1B0C), near the margin reddish orange (#CE4E24), towards the centre cherry red (#FE7C4D) to blood red (#6E1705), pale red (#FEB190) and pastel red (#F46733) when young, becoming cherry red (#FE7C4D) when mature. Lamellae 2–3 mm deep, adnate, dense, white (#F9F6E7) when young, becoming yellowish white (#F3F0CF) to pale yellow (#E4D39C) when mature; furcations absent, unequal with a few lamellulae of different lengths; edges concolorous and even. Stipe 25–40 × 10–17 mm, cylindrical or slightly thicker near the base, white (#F9F6E7), staining yellowish brown (#F5DD93) when bruised; medulla stuffed and becoming hollow when mature. Context 2–3 mm thick in a half of the pileus radius, pale yellow (#E4D39C) to yellow (#F3E392), yellow (#F3E392) to yellowish brown (#F5DD93) when bruised; odour fishy; taste mild. Spore print ochre.

Spores (5.0–)5.5–5.9–6.3(−6.6) × (4.0–)4.6–5.0–5.4(−5.6) μm, broadly ellipsoid, Q = (1.1–)1.13–1.18–1.23(−1.3); ornamentation of large, moderately distant [5–6(−6) in a 3 μm diam. circle] amyloid spines or warts, which are (0.7–)0.9–1.3(−1.4) μm high, isolated or fused in pairs or short chains [0–1(−2) fusions in the circle]; line connections absent or dispersed; suprahilar spot large, amyloid. Basidia (31–)31–36–41(−50) × (10–)10–11–12(−14) μm, clavate, 4-spored; basidiola first cylindrical, then clavate, 8.5–10.5 μm wide. Hymenial cystidia dispersed to moderately numerous, 300–1,100/mm2, (42–)53–59–64(−71) × (8–)9–10(−11) μm, mainly clavate or fusiform, apically acute, mucronate with a 1–9 μm long appendage, originating in subhymenium, thin-walled; contents completely heteromorphous crystalline, turning pale yellow-brown in sulfovanillin; abundant near the lamellae edges, (55–)58–62–65(−66) × (8–)9–10–11(−11) μm, similar to those on the sides. marginal cells (17–)20–23–26(−33) × (7–)8–9–10(−11) μm, undifferentiated. Pileipellis orthochromatic in Cresyl blue, sharply delimited from the underlying context, 220–450 μm deep, with a well-defined, strongly gelatinised, 70–120 μm deep suprapellis composed of ascending to erect hyphal terminations; subpellis 130–360 μm deep, composed of horizontally oriented, dense, intricate and narrow hyphae. Acid-resistant incrustations absent. Hyphal terminations near the pileus margin occasionally narrow, thin-walled; terminal cells (25–)33–47–60(−67) × (3–)3–4–5(−5) μm, cylindrical, apically obtuse or slightly constricted; subterminal cells usually equally long and wide, but often also shorter and wider, 1–2 μm wide. Hyphal terminations near the pileus centre similar, terminal cells even narrower, (38–)40–46–51(−58) × (3–)3–4(−4) μm; subterminal cells unbranched and embedded in intricate hyphae of the subpellis. Pileocystidia near the pileus margin very abundant, typically 1-celled, sometimes 2-celled, usually clavate, occasionally slightly flexuous, thin-walled, terminal cells variable in length, (59–)61–64–68(−72) × (5–)6–7–9(−10) μm, mostly subcylindrical or narrowly clavate, apically mainly obtuse, occasionally subacute, contents heteromorphous, usually dense and crystalline-granulose, turning grey-brown to black in sulfovanillin. Pileocystidia near the pileus centre slightly smaller; terminal cells (46–)50–60–70(−77) × (5–)5–6–8(−8) μm, mostly subclavate, cylindrical or fusiform, apically obtuse but occasionally also subacute to constricted. Cystidioid hyphae in subpellis and context dispersed, with heteromorphous granulose contents, oleiferous hyphae frequent in the lower part of subpellis and context.

Habit and habitat Solitary on soil in secondary broad-leaved forest (dominated by Quercus mongolica) at 300–500 m.

Other specimens examined CHINA. Jilin Province, Yanbian Korean Autonomous Prefecture, Wangqing County, Mantianxing National Forest Park, N 43°18′ E 129°45′, 381 m asl, 22 July 2016, Ming-Zhe Zhang, Xu-Ming Bai, Rong-Chun Dai, Guo-Jie Li, ZRL20162647 (HMAS279575); Jilin Province, Yanbian Korean Autonomous Prefecture, Wangqing County, Mantianxing National Forest Park, N 43°18′ E 129°45′, 381 m asl, 21 July 2016, Ming-Zhe Zhang, Xu-Ming Bai, Rong-Chun Dai, Guo-Jie Li, ZRL20162503 (HMAS279574).

Notes: According to the ITS phylogenetic tree (Figure 1), R. paragraveolens is phylogenetically related to R. amoenipes and R. graveolens. However, there are clear morphological differences, with R. paragraveolens having smaller spores and a brighter red pileus colour (Romagnesi 1967, 1985; Sarnari 1998; Sarnari and Redeuilh 2005). The new species R. paragraveolens is sister to R. pseudograveolens, both species belong to subsect. Xerampelinae of sect. Polychromae, but is morphologically distinct. Russula pseudograveolens is clearly distinguished from R. paragraveolens by having shorter and slender basidia [basidia of R. pseudograveolens (27.0–)28.5–30.4–32.3(−35.1) × (8.5–)9.1–9.7–10.2(−10.7) μm], longer projections of hymenial cystidia on lamellae sides [hymenial cystidia of R. pseudograveolens (41.3–)43.4–49.6–55.8(−64.1) × (5.4–)7.8–9.2–10.6(−10.3) μm], more lateral branches of hyphal terminations in pileipellis.

Russula pseudograveolens S.H. Wang, G.J. Li, R.L. Zhao & B. Cao, sp. nov., Figures 3b–f, 4 c–d, 7, 8, 13b

Figure 7.

Figure 7.

Russula pseudograveolens (HMAS287384, holotype), hymenium. (a) Basidia. (b) Basidiola. (c) Marginal cells on the lamella edges. (d) Hymenial cystidia near the lamella sides. (e) Hymenial cystidia on the lamella edges. Cystidia with contents as observed in Congo Red. Scale bar = 10 μm.

Figure 8.

Figure 8.

Russula pseudograveolens (HMAS287384, holotype), pileipellis. (a) Pileocystidia near the pileus centre. (b) Hyphal terminations near the pileus centre. (c) Pileocystidia near the pileus margin. (d) Hyphal terminations near the pileus margin. Cystidial contents as observed in Congo Red. Scale bar = 10 μm.

Fungal Names: FN571275.

Typification CHINA. Chongqing City, Chengkou County, Daba Mountain, Beiping Mountain, N 32°0′ E 108°44′, 1,570 m asl, 14 September 2021, Xin-Yu Zhu, Ming-Zhe Zhang, Yang Liu, Chen-Hao Li, ZRL20211703 (holotype HMAS287384). GenBank: OQ871496 (ITS), OQ875225 (nucLSU), OQ878264 (mtSSU), OQ933795 (rpb2), OQ948119 (tef1).

Etymology Named after its similarity to the species R. graveolens.

Diagnosis Pileus medium-sized, with violet brown to brownish red colour; lamellae with yellowish white to pale cream colour; stipe 22–24 × 8–10 mm, cylindrical, mainly pale brown; spores (5.5–)6.0–6.3–6.6(−6.9) × (4.7–)5.0–5.2–5.5(−5.7) μm, broadly ellipsoid, large; basidia (27–)28–30–32(−35) × (8.5–)9–10(−11) μm, clavate; hymenial cystidia (41–)43–50–56(−64) × (5–)8–9–11(−11) μm, mainly clavate or fusiform, apically acute; hyphal terminations near the pileus margin occasionally narrow, thin-walled, terminal cells mainly cylindrical, apically obtuse or slightly constricted. subterminal cells branched and embedded in intricate hyphae of the subpellis.

Pileus medium-sized, 40–47 mm diam., hemispherical when young, becoming applanate when mature, margin undulate, typically cracking when mature; near the centre darker and more brown (#56464F), violet brown (#6B5D6E) to brownish red (#623C47), near the margin pale red (#BD8791) to pastel red (#905361), cuticle dry, matt, minutely pruinose or encrusted with granulose tufts over entire surface which are darker than the background. Lamellae 2 mm deep, pale yellow (#C9CEC8), yellowish white (#F6FCFF) when young, yellowish white (#F6FCFF) to pale cream (#D0D3C8), adnate, dense, lamellulae and furcations absent; edges concolorous and even. Stipe 22–24 × 8–10 mm, cylindrical, mainly pale brown (#777671), near the lamellae yellowish white (#F6FCFF) to white (#C1CEED), medulla stuffed and becoming hollow when mature. Context 1 mm thick in a half of the pileus radius, yellowish white (#F6FCFF) to cream (#CDCDC3), yellow (#D2D5CA) to yellowish brown (#A29D83) when bruised; no distinct odour first, somewhat fishy when dry; taste mild. Spore print not observed.

Spores (5.5–)6.0–6.3–6.6(−6.9) × (4.7–)5.0–5.2–5.5(−5.7) μm, broadly ellipsoid, Q = (1.1–)1.18–1.20–1.23(−1.3); ornamentation of large, dense [7–8(−8) in a 3 μm diam. circle] amyloid spines or warts, which are (0.6–)0.7–0.9(−1.0) μm high, isolated or fused in pairs or short chains [0–1(−2) fusions in the circle]; line connections absent or dispersed; suprahilar spot large, amyloid. Basidia (27–)28–30–32(−35) × (8.5–)9–10(−11) μm, clavate, 4-spored; basidiola first cylindrical, then clavate, 6.8–8.6 μm wide. Hymenial cystidia dispersed to moderately numerous, 300–1,100/mm2, (41–)43–50–56(−64) × (5–)8–9–11(−11) μm, mainly clavate or fusiform, apically acute, mucronate with a 6–10 μm long appendage, originating in subhymenium, thin-walled; contents completely heteromorphous crystalline, turning pale yellow-brown or pale greyish brown in sulfovanillin; abundant near the lamellae edges, (42–)42–48–54(−63) × (6–)6–7(−8) μm, similar to those on the sides but usually smaller. Marginal cells (13–)13–15–18(−19) × (5–)5–6–7(−8) μm, undifferentiated. Pileipellis orthochromatic in Cresyl blue, sharply delimited from the underlying context, 200–320 μm deep, with a well-defined, strongly gelatinised, 80–120 μm deep suprapellis composed of ascending to erect hyphal terminations; subpellis 110–200 μm deep, composed of horizontally oriented, dense, intricate and narrow hyphae. Acid-resistant incrustations absent. Hyphal terminations near the pileus margin occasionally narrow, thin-walled; terminal cells (36–)37–53–69(−83) × (1.6–)2.0–2.4–2.9(−3.0) μm, cylindrical, apically obtuse or slightly constricted; subterminal cells usually equally long and wide, but often also shorter and wider, 1–2 μm wide, branched or not. Hyphal terminations near the pileus centre similar, terminal cells even narrower, (28–)32–37–42(−43) × (1.5–)1.9–2.7–3.4(−3.7) μm; subterminal cells branched and embedded in intricate hyphae of the subpellis. Pileocystidia near the pileus margin very abundant, typically 1-celled, sometimes 2-celled, usually clavate, occasionally slightly flexuous, thin-walled, terminal cells variable in length, (48–)49–54–59(−60) × (4.2–)4.7–5.3–5.9(−5.9) μm, mostly subcylindrical or narrowly clavate, apically mainly obtuse, occasionally subacute, contents heteromorphous, usually dense and crystalline-granulose, turning grey-brown to black in sulfovanillin. Pileocystidia near the pileus centre slightly smaller; terminal cells (43–)47–51–55(−58) × (3.4–)4.0–4.8–5.6(−5.7) μm, mostly subclavate, cylindrical or fusiform, apically obtuse but occasionally also subacute to constricted. Cystidioid hyphae in subpellis and context dispersed, with heteromorphous granulose contents, oleiferous hyphae frequent in the lower part of subpellis and context.

Habit and habitat Solitary on soil in mixed coniferous and broad-leaved forest (dominated by Fagaceae spp. of Castanopsis, Lithocarpus, and Quercus, intermixed with Pinus yunnanensis var. tenuifolia) at 500–2,200 m.

Other specimens examined CHINA. Chongqing City, Chengkou County, Daba Mountain, Beiping Mountain, N 32°0′ E 108°44′, 1,570 m asl, 14 September 2021, Xin-Yu Zhu, Ming-Zhe Zhang, Yang Liu, Chen-Hao Li, ZRL20211685 (HMAS287385); Guangxi Zhuang Autonomous Region, Baise City, Leye County, Yachang Orchid National Nature Reserve, N 24°44′ E 106°19′, 1,211 m asl, 6 August 2017, Rui-Lin Zhao, GX20170438 (HMAS279577); Guangxi Zhuang Autonomous Region, Baise City, Leye County, Yachang Orchid National Nature Reserve, N 24°44′ E 106°19′, 1,211 m asl, 6 August 2017, Hui-Jun Wang, GX20170498 (HMAS279579).

Notes: According to the ITS phylogenetic tree (Figure 1), R. pseudograveolens is phylogenetically related to R. graveolens. However, there are clear morphological differences, with R. pseudograveolens having smaller spores, shorter basidia, and a brighter red pileus colour (Romagnesi 1967, 1985; Sarnari 1998; Sarnari and Redeuilh 2005). The new species R. pseudograveolens is sister to R. paragraveolens. However, differences not only in morphology, but also in host plants and geographical distribution. Russula paragraveolens grows solitarily on the ground in secondary broadleaved forest (dominated by Quercus mongolica) at 300–500 m, while R. pseudograveolens grows at higher altitudes and has more complex host plants at 500–2,200 m. Furthermore, R. paragraveolens and R. pseudograveolens belong to different temperature zones, the former being a temperate species and the latter a subtropical species.

Russula shigatseensis S.H. Wang, R.L. Zhao & B. Cao, sp. nov., Figures 3k–o, 4g–h, 9, 10, 13c

Figure 9.

Figure 9.

Russula shigatseensis (HMAS287389, holotype), hymenium. (a) Basidia. (b) Basidiola. (c) Marginal cells on the lamella edges. (d) Hymenial cystidia near the lamella sides. (e) Hymenial cystidia on the lamella edges. Cystidia with contents as observed in Congo Red. Scale bar = 10 μm.

Figure 10.

Figure 10.

Russula shigatseensis (HMAS287389, holotype), pileipellis. (a) Pileocystidia near the pileus centre. (b) Hyphal terminations near the pileus centre. (c) Pileocystidia near the pileus margin. (d) Hyphal terminations near the pileus margin. Cystidial contents as observed in Congo Red. Scale bar = 10 μm.

Fungal Names: FN571577.

Typification CHINA. Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, N 27°25′ E 88°56′, 3,024 m asl, 26 July 2022, Rui-Lin Zhao, Xin-Yu Zhu, Jia-Xin Li, ZRL20220194 (holotype HMAS287389). GenBank: OQ871501 (ITS), OQ875230 (nucLSU), OQ878269 (mtSSU), OQ933787 (rpb2), OQ948114 (tef1).

Etymology Refers to Shigatse Municipality, the locality of the type specimen.

Diagnosis Pileus medium-sized, with brownish orange to madder red colour; lamellae with yellowish white to pale cream colour; stipe 45–104 × 12–18 mm, cylindrical and slightly thick near the base; spores (5.6–)6.0–6.4–6.9(−7.5) × (4.8–)5.2–5.7–6.2(−6.7) μm, subglobose, medium-sized; basidia (24–)31–35–39(−39) × (8–)10–12–13(−13) μm, clavate; hymenial cystidia (64–)69–78–87(−97) × (5–)6–7–8(−8) μm, mainly clavate or fusiform, apically acute; hyphal terminations near the pileus margin occasionally narrow, thin-walled, terminal cells mainly cylindrical, apically obtuse or slightly constricted. subterminal cells branched and embedded in intricate hyphae of the subpellis.

Pileus medium-sized, 59–80 mm diam., hemispherical when young, becoming applanate with depressed centre when mature, applanate with depressed centre; margin smooth; cuticle dry to viscid, smooth, peeling to 1/2 of the radius, brownish orange (#B66747) to madder red (#C43925) in the centre, pinkish red (#E68A99) towards the margin. Lamellae 1–7 mm deep, yellowish white (#A19D87) to white (#CED0CD) when young, yellowish white (#A19D87) to pale cream (#CAD0C9), adnate, dense, lamellulae and furcations absent; edges concolorous and even. Stipe 45–104 × 12–18 mm, cylindrical and slightly thick near the base, white (#CED0CD), often with pinkish flush or pink areas, medulla stuffed and becoming hollow when mature. Context 1–2 mm thick in a half of the pileus radius, yellowish white (#A19D87) to cream (#C1BDBA). Spore print not observed

Spores (5.6–)6.0–6.4–6.9(−7.5) × (4.8–)5.2–5.7–6.2(−6.7) μm, subglobose, Q = (1.0–)1.0–1.13–1.18(−1.3); ornamentation of medium-sized, moderately distant to dense [6–8 (−12) in a 3 μm diam. circle] amyloid spines or warts, which are (0.5–)0.5–0.7(−0.8) μm high, isolated or fused in pairs or short chains [0–1(−2) fusions in the circle]; line connections absent or dispersed; suprahilar spot large, amyloid. Basidia (24–)31–35–39(−39) × (8–)10–12–13(−13) μm, clavate, 4-spored; basidiola first cylindrical, then clavate, 7.0–10.7 μm wide. Hymenial cystidia dispersed to moderately numerous, 300–1,100/mm2, (64–)69–78–87(−97) × (5–)6–7–8(−8) μm, mainly clavate or fusiform, apically acute, mucronate with a 0–5 μm long appendage, originating in subhymenium, thin-walled; contents completely heteromorphous crystalline, turning grey-brown to black in sulfovanillin; abundant near the lamellae edges, (49–)50–58–65(−77) × (3–)5–6–7(−8) μm, similar to those on the sides but usually smaller. Marginal cells (9–)8–12–16(−21) × (4–)3–5–6(−9) μm, undifferentiated. Pileipellis orthochromatic in Cresyl blue, sharply delimited from the underlying context, 140–330 μm deep, with a well-defined, strongly gelatinised, 50–150 μm deep suprapellis composed of ascending to erect hyphal terminations; subpellis 90–180 μm deep, composed of horizontally oriented, dense, intricate and narrow hyphae. Acid-resistant incrustations absent. Hyphal terminations near the pileus margin occasionally narrow, thin-walled; terminal cells (44–)57–86–116(−142) × (2.5–)3–4–5(−5) μm, cylindrical, apically obtuse or slightly constricted; subterminal cells usually equally long and wide, but often also shorter and wider, 1–2 μm wide, branched or not. Hyphal terminations near the pileus centre similar, terminal cells even narrower, (26–)29–38–46(−56) × (1.0–)1.3–1.9–2.5(−3.2) μm; subterminal cells branched and embedded in intricate hyphae of the subpellis. Pileocystidia near the pileus margin very abundant, typically 1–2-celled, seldom 3–4-celled, usually clavate, frequently slightly flexuous, thin-walled, terminal cells variable in length, (36–)40–46–52(−55) × (2.5–)2.9–3.4–4.0(−4.4) μm, mostly subcylindrical or narrowly clavate, apically mainly obtuse, occasionally subacute, contents heteromorphous, usually dense and crystalline-granulose, turning pale yellow-brown or pale greyish brown in sulfovanillin. Pileocystidia near the pileus centre slightly smaller; terminal cells (25–)28–35–41(−46) × (2.5–)2.7–3.2–3.7(−3.8) μm, mostly subclavate, cylindrical or fusiform, apically obtuse but occasionally also subacute to constricted. Cystidioid hyphae in subpellis and context dispersed, with heteromorphous granulose contents, oleiferous hyphae frequent in the lower part of subpellis and context.

Habit and habitat: Scattered in coniferous forests.

Other specimens examined CHINA. Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, N 27°25′ E 88°56′, 3,024 m asl, 26 July 2022, Mao-Qiang He, Bin Cao, ZRL20220072 (HMAS287390); Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, N 27°25′ E 88°56′, 3,024 m asl, 26 July 2022, Mao-Qiang He, Bin Cao, ZRL20220207 (HMAS287391).

Notes: According to the ITS and multigene phylogeny, R. shigatseensis belonging to sect. Flavisiccantes, subsect. Lepidinae, is represented in a well-supported clade (BS = 100%) by three specimens from the Shigatse region of Xizang, China. The species is closely related to R. lepida Fr., but R. shigatseensis has smaller spores [(5.6–)6.0–6.4–6.9(−7.5) × (4.8–)5.2–5.7–6.2(−6.7) μm]. Compared to R. lepida [2–9 × 4–7 μm], the spores of R. shigatseensis have spore ornamentations of more or less isolated spines (Sarnari and Redeuilh 2005). R. flavisiccans Bills also appeared close to the present species in multigene phylogeny but the former differs from newly proposed species in having adnate to notched, forked, or anastomosing lamellae with scattered lamellulae, larger spores [7–8.5(−9) × 6.5–8(−8.5) μm] (Bills 1989).

Russula yadongensis S.H. Wang, R.L. Zhao & B. Cao, sp. nov., Figures 3g–j, 4e–f, 11, 12, 13d

Figure 11.

Figure 11.

Russula yadongensis (HMAS287386, holotype), hymenium. (a) Basidia. (b) Basidiola. (c) Marginal cells on the lamella edges. (d) Hymenial cystidia near the lamella sides. (e) Hymenial cystidia on the lamella edges. Cystidia with contents as observed in Congo Red. Scale bar = 10 μm.

Figure 12.

Figure 12.

Russula yadongensis (HMAS287386, holotype), pileipellis. (a) Pileocystidia near the pileus centre. (b) Hyphal terminations near the pileus centre. (c) Pileocystidia near the pileus margin. (d) Hyphal terminations near the pileus margin. Cystidial contents as observed in Congo Red. Scale bar = 10 μm.

Fungal Names: FN571578.

Typification CHINA. Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, N 27°25′ E 88°56′, 26 July 2022, 3,024 m asl, Mao-Qiang He, Bin Cao, ZRL20220204 (holotype HMAS287386). GenBank: OQ871498 (ITS), OQ875228 (nucLSU), OQ878267 (mtSSU), OQ933790 (rpb2), OQ948117 (tef1).

Etymology Refers to Yadong County, the locality of the type specimen.

Diagnosis Pileus medium-sized, light purple to purple, dark purplish red with brownish purple tints in the centre; lamellae with yellowish white to pale yellow colour; stipe 37–66 × 5–15 mm, cylindrical and slightly thick near the base; spores (6.0–)6.3–6.6–7.0(−7.2) × (4.5–)5.0–5.4–5.8(−6.2) μm, broadly ellipsoid, large; basidia (21–)22–24–26(−28) × (10–)10–11(−11) μm, clavate; hymenial cystidia (40–)35–41–46(−58) × (7–)7–8–9(−11) μm, mainly clavate or fusiform, apically acute; Hyphal terminations near the pileus margin occasionally narrow, thin-walled; terminal cells cylindrical, apically obtuse or slightly constricted; subterminal cells unbranched.

Pileus medium-sized, 32–46 mm diam., applanate with depressed centre; margin smooth or slightly striate; cuticle smooth and shiny, peeling to 1/3 of the radius, light purple (#CAB5B1) when young, purple (#996F7F) when mature, dark purplish red (#7B5E6A) with brownish purple tints in the centre. Lamellae 2–4 mm deep, adnate to free, dense, white (#D0D6E7) when young, becoming yellowish white (#D1DCD8) to pale yellow (#EBF6FA) when mature; lamellulae and furcations absent; edges concolorous and even. Stipe 37–66 × 5–15 mm, cylindrical and slightly thick near the base, white (#D0D6E7); medulla stuffed and becoming hollow when mature. Context 1–2 mm thick in a half of the pileus radius, white (#D0D6E7), yellowish white (#D1DCD8) to cream (#D7E0DF) when mature. Spore print not observed.Spores (6.0–)6.3–6.6–7.0(−7.2) × (4.5–)5.0–5.4–5.8(−6.2) μm, broadly ellipsoid, Q = (1.1–)1.15–1.23–1.3(−1.4); ornamentation of large, moderately distant [5–6(−7) in a 3 μm diam. circle] amyloid spines or warts, which are (0.7–)0.9–1.2(−1.3) μm high, isolated or fused in pairs or short chains [0–1(−2) fusions in the circle]; line connections absent or dispersed; suprahilar spot large, amyloid. Basidia (21–)22–24–26(−28) × (10–)10–11(−11) μm, clavate, 4-spored; basidiola first cylindrical, then clavate, 7.2–9.1 μm wide. Hymenial cystidia dispersed to moderately numerous, 300–1,100/mm2, (40–)35–41–46(−58) × (7–)7–8–9(−11) μm, mainly clavate or fusiform, apically acute, mucronate with a 0–6 μm long appendage, originating in subhymenium, thin-walled; contents completely heteromorphous crystalline, turning pale yellow-brown or pale greyish brown in sulfovanillin; abundant near the lamellae edges, (30–)44–53–61(−58) × (5–)7–9–10(−11) μm, similar to those on the sides. Marginal cells (9–)12–15–17(−18) × (6–)6–8–9(−10) μm, undifferentiated. Pileipellis orthochromatic in Cresyl blue, sharply delimited from the underlying context, 160–360 μm deep, with a well-defined, strongly gelatinised, 60–140 μm deep suprapellis composed of ascending to erect hyphal terminations; subpellis 100–220 μm deep, composed of horizontally oriented, dense, intricate and narrow hyphae. Acid-resistant incrustations absent. Hyphal terminations near the pileus margin occasionally narrow, thin-walled; terminal cells (26–)25–41–56(−81) × (2–)2–3(−3) μm, cylindrical, apically obtuse or slightly constricted; subterminal cells usually equally long and wide, but often also shorter and wider, 1–2 μm wide. Hyphal terminations near the pileus centre similar, terminal cells even narrower, (25–)27–34–40(−45) × (1.2–)1.5–2.0–2.4(−2.6) μm; subterminal cells unbranched and embedded in intricate hyphae of the subpellis. Pileocystidia near the pileus margin very abundant, typically 1–2-celled, sometimes 2–3-celled, usually clavate, occasionally slightly flexuous, thin-walled, terminal cells variable in length, (31–)33–56–78(−103) × (3.5–)3.7–4.9–6.2(−7.8) μm, mostly subcylindrical or narrowly clavate, apically mainly obtuse, occasionally subacute, contents heteromorphous, usually dense and crystalline-granulose, turning grey-brown to black in sulfovanillin. Pileocystidia near the pileus centre slightly smaller; terminal cells (30–)33–44–55(−63) × (2.6–)3.7–4.6–5.6(−6.5) μm, mostly subclavate, cylindrical or fusiform, apically obtuse but occasionally also subacute to constricted. Cystidioid hyphae in subpellis and context dispersed, with heteromorphous granulose contents, oleiferous hyphae frequent in the lower part of subpellis and context.

Habit and habitat: Scattered in coniferous forests.

Other specimens examined CHINA. Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, N 27°22′ E 88°58′, 2,872 m asl, 26 July 2022, Rui-Lin Zhao, Xin-Yu Zhu, Jia-Xin Li, ZRL20220152 (HMAS287387); Xizang Autonomous Region, Shigatse Municipality, Yadong County, Lower Yadong Township, Yanqinggang Village, N 27°25′ E 88°55′, 3,254 m asl, 27 July 2022, Mao-Qiang He, Bin Cao, ZRL20220377 (HMAS287388).

Notes: Russula yadongensis belonging to subsect. Laricinae of sect. Tenellae, is represented by three specimens from the Shigatse region of Xizang, China in a well-supported clade (BS = 97%), and is phylogenetically related to R. sichuanensis G.J. Li & H.A. Wen and R. vinosobrunneola G.J. Li & R.L. Zhao (Figure 1). However, there are clear morphological differences, with R. yadongensis having smaller spores [(6.0–)6.3–6.6–7.0(−7.2) × (4.5–)5.0–5.4–5.8(−6.2) μm], a deeper purple pileus colour. Compared with R. vinosobrunneola and R. sichuanensis, the spores of R. yadongensis have spore ornamentations of more or less isolated spines (Li et al. 2018a). Russula yadongensis is also closely related to R. nauseosa (Pers.) Fr. and R. laricina Fr. in the multigene phylogeny (Figure 2). Compared to the closely related species R. nauseosa, the spores of R. yadongensis are smaller [spores of R. nauseosa 7,8–10 × 6,6–7,8 μm] and the hymenial cystidia are slightly smaller [hymenial cystidia of R. nauseosa 45–80 × 9–13 μm] (Sarnari and Redeuilh 2005). Compared to the closely related species R. laricina, the spores of R. yadongensis are smaller [spores of R. laricina 6,5–9,5 × 6–8 μm] and have a deeper purple pileus colour (Sarnari and Redeuilh 2005).

4. Discussion

The ITS phylogenetic analyses are most commonly used for the practical identification of Russula species (Li et al. 2019). However, it is often difficult to distinguish between closely related species based on ITS phylogenetic analysis alone. Multi-locus phylogenetic analyses have become the preferred technique for revealing relationships within the Russula genus in recent years (Li et al. 2019; Buyck et al. 2020). In this study, the topological structure of the ITS and multi-locus phylogenetic analyses are basically similar, but the Bayesian posterior probability values and maximum likelihood bootstrap were higher in the multi-locus phylogenetic analyses.

In this study, four new species belong to three different subsections within the crown clade, namely subsect. Laricinae (R. yadongensis), subsect. Lepidinae (R. shigatseensis), subsect. Xerampelinae (R. paragraveolens and R. pseudograveolens). In China, some new species of these three subsections have previously been reported, such as R. cessans, R. faginea, R. laricina, R. lepida, R. nauseosa, R. nuoljae, R. pascua, R. sichuanensis, R. vinosobrunneola, R. xerampelina (Li 2014; Li et al. 2018b; Cao et al. 2019).

Species of subsect. Laricinae generally have a purple pileus, white stipe, and a yellow spore print, and mainly grow in coniferous forests (Romagnesi 1967). Many species of this subsection have previously been reported, namely R. adwanitekae A. Ghosh, K. Das & Buyck, R. cessans A. Pearson, R. curtipes F.H. Møller & Jul. Schäff., R. laricina, R. nauseosa, R. obscurozelleri Bazzic., D. Mill. & Buyck, R. pseudotsugarum Bazzic., D. Mill. & Buyck, R. sichuanensis, R. vidalii Trappe & T.F. Elliott, R. vinaceodora (Calonge & J.M. Vidal) Trappe & T.F. Elliott, R. vinosobrunneola, R. zelleri Burl (Ghosh et al. 2021). In this study, ITS phylogenetic analyses showed significant support (BS = 93%) for R. yadongensis with other species in this subsection, while morphological and phylogenetic results could distinguish this species well from other known species within this subsection.

Subsection Lepidinae is characterised by a velvety pileus surface, hard context, the cystidia of the pileus, and hymenium not reacting to sulfovanillin, mild taste (Sarnari and Redeuilh 2005). Many species of subsect. Lepidinae have previously been reported, namely R. amarissima Romagn. & E.-J. Gilbert, R. Baniyakundensis A. Ghosh, K. Das & D. Chakr., R. flavisiccans, R. indoarmeniaca A. Ghosh, K. Das & R.P. Bhatt, R. lepida, R. ochroleucoides Kauffman (Kauffman 1917; Bills 1989; Sarnari and Redeuilh 2005; Ghosh et al. 2016, 2021). In this study, ITS phylogenetic analyses showed significant support (BS = 100%) for R. shigatseensis with other species in this subsection, while morphological and phylogenetic results could distinguish this species well from other known species within this subsection.

Species of the subsect. Xerampelinae can be easily recognised in field by following characters: tardily fishy context smell, mild taste, context slowly turning brownish when bruised or old, lamellae turning red in aniline, absence of acid-resistant incrustation on pileocystidia which turn grey in sulphovanillin (Adamczík and Marhold 2000; Adamcik 2002, 2003; Adamčík 2004; Adamčik and Knudsen 2004; Sarnari and Redeuilh 2005; Buyck and Adamcík 2013; Adamčík et al. 2016). Many species in this subsection have previously been reported, such as R. faginea Romagn., R. favrei M.M. Moser, R. clavipes Velen., R. graveolens, R. nuoljae Kühner, R. pascua (F.H. Møller & Jul. Schäff.) Kühner, R. subrubens (J.E. Lange) Bon, and R. xerampelina (Schaeff.) Fr (Adamčík et al. 2016). In this study, ITS phylogenetic analyses showed significant support (BS = 97%) for R. paragraveolens and R. pseudograveolens with other species in this subsection, while morphological and phylogenetic results could distinguish this species well from other known species within this subsection.

Acknowledgments

We thank Chun-Rong Dai, Hui-Jun Wang, Xu-Ming Bai, Yan-Lei Ding, Zhi-Lin Ling, Hu-Sheng Ma, Guang-Fu Mou, Chen-Hao Li, and Yang Liu for assistance in specimen collecting.

Funding Statement

This project was supported by the Survey of Wildlife Resources in Key Areas of Tibet (ZL202203601), the National Natural Science Foundation of China (31961143010, 31500013, 30770013), the Beijing Innovation Consortium of Agriculture Research System (BAIC03-01), the Talent Introduction Scientific Research Special Project of Hebei Agricultural University (YJ201849), and the Projects of Science and Technology Programs of Tibet (XZ202202YD0031C).

Disclosure statement

No potential conflict of interest was reported by the author(s).

References

  1. Adamcik S. 2002. Taxonomy of the Russula xerampelina group. Part 2. Taxonomic and nomenclatural study of Russula xerampelina and R. erythropoda. Mycotaxon. 82:241–267. [Google Scholar]
  2. Adamcik S. 2003. Russula faginea and similar taxa. Czech Mycol. 55:177–192. doi: 10.33585/cmy.54306. [DOI] [Google Scholar]
  3. Adamčík S. 2004. Studies on Russula lavipes and related taxa of Russula section Xerampelinae with a predominantly olivaceous pileus. Persoonia. 18:393–409. [Google Scholar]
  4. Adamčik S, Knudsen H. 2004. Red-capped species of Russula sect. Xerampelinae associated with dwarf scrub. Xerampelinae Assoc Dwarf Scrub Mycol Res. 108(12):1463–1475. doi: 10.1017/S0953756204000875. [DOI] [PubMed] [Google Scholar]
  5. Adamčík S, Looney B, Caboň M, Jančovičová S, Adamčíková K, Avis PG, Barajas M, Bhatt RP, Corrales A, Das K. 2019. The quest for a globally comprehensible Russula language. Fungal Divers. 99:369–449. doi: 10.1007/s13225-019-00437-2. [DOI] [Google Scholar]
  6. Adamčík S, Slovák M, Eberhardt U, Ronikier A, Jairus T, Hampe F, Verbeken A. 2016. Molecular inference, multivariate morphometrics and ecological assessment are applied in concert to delimit species in the Russula clavipes complex. Mycologia. 108:716–730. doi: 10.3852/15-194. [DOI] [PubMed] [Google Scholar]
  7. Adamczík S, Marhold K. 2000. Taxonomy of the Russula xerampelina group I. Morphometric study of the Russula xerampelina group in Slovakia. Mycotaxon. 76:463–479. [Google Scholar]
  8. Andrew R 2016. Tree drawing tool version 1.4.3. Edinburgh, UK: Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/. [Google Scholar]
  9. Bills GF. 1989. Southern Appalachian Russulas. IV. Mycologia. 81:57–65. doi: 10.1080/00275514.1989.12025626. [DOI] [Google Scholar]
  10. Buyck B. 1989. Valeur taxonomique du bleu de crésyl pour le genre Russula [Taxonomic value of cresyl blue for the genus Russula]. Bull Soc Mycol Fr. 105:1–6. [Google Scholar]
  11. Buyck B, Adamcík S. 2013. The Russula xerompelina complex Russulales, Agaricomycotina in North America. Scr Bot Belg. 51:117–131. [Google Scholar]
  12. Buyck B, Wang X, Adamcíková K, Cabon M, Jancovicova S, Hofstetter V, Adamcik S. 2020. One step closer to unravelling the origin of Russula: subgenus glutinosae subg. nov. Mycosphere. 11(1):285–304. doi: 10.5943/mycosphere/11/1/6. [DOI] [Google Scholar]
  13. Buyck B, Zoller S, Hofstetter V. 2018. Walking the thin line… ten years later: the dilemma of above- versus below-ground features to support phylogenies in the Russulaceae (Basidiomycota). Fungal Divers. 89(1):267–292. doi: 10.1007/s13225-018-0397-5. [DOI] [Google Scholar]
  14. Caboň M, Eberhardt U, Looney B, Hampe F, Kolařík M, Jančovičová S, Verbeken A, Adamčík S. 2017. New insights in Russula subsect. Rubrinae: phylogeny and the quest for synapomorphic characters. Mycol Prog. 16(9):877–892. doi: 10.1007/s11557-017-1322-0. [DOI] [Google Scholar]
  15. Caboň M, Li GJ, Saba M, Kolařík M, Jančovičová S, Khalid AN, Moreau PA, Wen HA, Pfister DH, Adamčík S. 2019. Phylogenetic study documents different speciation mechanisms within the Russula globispora lineage in boreal and arctic environments of the Northern Hemisphere. IMA Fungus. 10:1–16. doi: 10.1186/s43008-019-0003-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Cao B, Li GJ, Zhao RL. 2019. Species diversity and geographic components of Russula from the greater and Lesser Khinggan Mountains. Biodiversity Sci. 27:854. doi: 10.17520/biods.2019040. [DOI] [Google Scholar]
  17. Chen XJ, Zhang YJ. 2010. Polysaccharide extract from Russula and its role of lowering blood glucose and lipid. Food Sci. 31:255–258. [Google Scholar]
  18. Chen Z, Zhang P, Zhang Z. 2014. Investigation and analysis of 102 mushroom poisoning cases in Southern China from 1994 to 2012. Fungal Divers. 64:123–131. doi: 10.1007/s13225-013-0260-7. [DOI] [Google Scholar]
  19. Cho JT, Han JH. 2016. A case of mushroom poisoning with Russula subnigricans: development of rhabdomyolysis, acute kidney injury, cardiogenic shock, and death. J Korean Med Sci. 31:1164–1167. doi: 10.3346/jkms.2016.31.7.1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ghosh A, Das K, Adhikari S, Bhatt R. 2016. A novel species of Russula (Russulaceae) from Indian Himalaya. Mycosphere. 7(6):778–785. doi: 10.5943/mycosphere/7/6/8. [DOI] [Google Scholar]
  21. Ghosh A, Das K, Buyck B. 2021. Two new species in the Russula (Russulaceae, Basidiomycota) crown clade from Indian Himalaya. Eur J Taxon. 782:157–172. doi: 10.5852/ejt.2021.782.1595. [DOI] [Google Scholar]
  22. Ghosh A, Das K, Chakraborty D. 2021. Morphology and molecular approach reveal a new species of the genus Russula subsect. Lepidinae (Russulaceae) from India. Lepidiane Russ India Phytox. 483(3):244–254. doi: 10.11646/phytotaxa.483.3.4. [DOI] [Google Scholar]
  23. Heilmann-Clausen J, Verbeken A, Vesterholt J, Leonard P. 2000. The genus Lactarius: book review. Field Mycol. 1(1):6–6. doi: 10.1016/S1468-1641(10)60005-9. [DOI] [Google Scholar]
  24. He MQ, Zhao RL, Hyde KD, Begerow D, Kemler M, Yurkov A, Mckenzie E, Raspe O, Kakishima M, Sanchez-Ramrez S. 2019. Notes, outline and divergence times of Basidiomycota. Fungal Divers. 99(1):105–367. doi: 10.1007/s13225-019-00435-4. [DOI] [Google Scholar]
  25. Jiang XM, Li YK, Liang JF, Wu JR. 2018. Russula brunneovinacea sp nov., from northeastern China. Mycotaxon. 132(4):789–797. doi: 10.5248/132.789. [DOI] [Google Scholar]
  26. Kaewnarin K, Suwannarach N, Kumla J, Lumyong S. 2016. Phenolic profile of various wild edible mushroom extracts from Thailand and their antioxidant properties, anti-tyrosinase and hyperglycaemic inhibitory activities. J Funct Foods. 27:352–364. doi: 10.1016/j.jff.2016.09.008. [DOI] [Google Scholar]
  27. Kalyaanamoorthy S, Minh BQ, WongThomas KF, Haeseler V, Jermiin A, Lars S. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 14(6):587–589. doi: 10.1038/nmeth.4285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kauffman CH. 1917. Tennessee and Kentucky fungi. Mycologia. 9:159–166. doi: 10.1080/00275514.1917.12018913. [DOI] [Google Scholar]
  29. Khatua S, Gupta SS, Ghosh M, Tripathi S, Acharya K. 2021. Exploration of nutritional, antioxidative, antibacterial and anticancer status of Russula alatoreticula: towards valorization of a traditionally preferred unique myco-food. J Food Sci Technol. 58:2133–2147. doi: 10.1007/s13197-020-04723-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Ainsworth & Bisby's Dictionary of the Fungi. 10th ed. Wallingford: CABI. [Google Scholar]
  31. Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol. 34:772–773. doi: 10.1093/molbev/msw260. [DOI] [PubMed] [Google Scholar]
  32. Li GJ. 2014. The Taxonomy of Russula in China. Beijing: University of Chinese Academy of Sciences. [Google Scholar]
  33. Li GJ. 2022. Russula rubiginosus sp. nov. In Russula subsect. maculatinae from Heilongjiang Province, Northeast China. Phytotaxa. 575(2):140–148. doi: 10.11646/phytotaxa.575.2.3. [DOI] [Google Scholar]
  34. Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-Wahab MA, Alvarado P, Alves-Silva G, Ammirati JF, Ariyawansa HA, et al. 2016. Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers. 78:1–237. doi: 10.1007/s13225-016-0366-9. [DOI] [Google Scholar]
  35. Li GJ, Li SF, Liu XZ, Wen HA. 2012. Russula jilinensis sp. nov. (Russulaceae) from Northeast China. Mycotaxon. 120:49–58. doi: 10.5248/120.49. [DOI] [Google Scholar]
  36. Li F, Li GJ, Zhang J, Gao H, Shi RS, Deng CY. 2021. Russula fanjing, a new species of Russula subsect. Russula (Russulaceae, Russulales) from Guizhou province, China. Phytotaxa. 480:139–151. doi: 10.11646/phytotaxa.480.2.3. [DOI] [Google Scholar]
  37. Li YK, Xin Z, Yuan Y, Cao Z, Liang JF. 2015. Morphological and molecular evidence for a new species of Russula (Russulaceae) from southern China. Phytotaxa. 202(2):94–102. doi: 10.11646/8466. [DOI] [Google Scholar]
  38. Li GJ, Zhang CL, Zhao RL, Lin FC. 2018a. Two new species of Russula from Northeast China. Mycosphere. 9(3):431–443. doi: 10.5943/mycosphere/9/3/1. [DOI] [Google Scholar]
  39. Li GJ, Zhang C, Zhao RL, Lin FC. 2018b. Hypogeous gasteroid lactarius sulphosmus sp. nov. and agaricoid Russula vinosobrunneola sp. nov. (Russulaceae) from China. Mycosphere. 9(4):838–858. doi: 10.5943/mycosphere/9/4/9. [DOI] [Google Scholar]
  40. Li GJ, Zhao D, Li SF, Yang HJ, Liu XZ. 2013a. Russula changbaiensis sp. nov. From northeast China. Mycotaxon. 124:269–278. doi: 10.5248/124.269. [DOI] [Google Scholar]
  41. Li GJ, Zhao RL, Zhang CL, Lin FC. 2019. A preliminary DNA barcode selection for the genus Russula (Russulales, Basidiomycota). Mycology. 10:61–74. doi: 10.1080/21501203.2018.1500400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Li GJ, Zhao Q, Zhao D, Yue SF, Li SF, Wen HA, Liu XZ. 2013b. Russula atroaeruginea and R. sichuanensis spp. nov. From southwest China. Mycotaxon. 124(1):173–188. doi: 10.5248/124.173. [DOI] [Google Scholar]
  43. Liu L, Liu Z, Y Q, Sui Z, Peng N, Y Y, Zang Y, Wang X, Zhou L, Y Q, et al. 2023. Research progress on nutritional function and bioactivities of Russula. Sci Technol Food Ind. 44:447–453. doi: 10.13386/j.issn1002-0306.2022030358. [DOI] [Google Scholar]
  44. Looney BP, Meidl P, Piatek MJ, Miettinen O, Martin FM, Matheny PB, Labbé JL. 2018. Russulaceae: a new genomic dataset to study ecosystem function and evolutionary diversification of ectomycorrhizal fungi with their tree associates. New Phytol. 218:54–65. doi: 10.1111/nph.15001. [DOI] [PubMed] [Google Scholar]
  45. Looney BP, Ryberg M, Hampe F, Sánchez‐García M, Matheny PB. 2015. Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi. Mol Ecol. 25(2):630–647. doi: 10.1111/mec.13506. [DOI] [PubMed] [Google Scholar]
  46. Matheny PB. 2005. Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol. 35:1–20. doi: 10.1016/j.ympev.2004.11.014. [DOI] [PubMed] [Google Scholar]
  47. Matsuura M, Kato S, Saikawa Y, Nakata M, Hashimoto K. 2016. Identification of cyclopropylacetyl-(R)-carnitine, a unique chemical Marker of the fatally toxic mushroom Russula subnigricans. Chem Pharm Bull. 64(6):602–608. doi: 10.1248/cpb.c15-01033. [DOI] [PubMed] [Google Scholar]
  48. Moncalvo JM, Lutzoni FM, Rehner SA, Johnson J, Vilgalys R. 2000. Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences. Syst Biol. 49:278–305. doi: 10.1093/sysbio/49.2.278. [DOI] [PubMed] [Google Scholar]
  49. Rehner SA, Buckley E. 2005. A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia. 97(1):84–98. doi: 10.1080/15572536.2006.11832842. [DOI] [PubMed] [Google Scholar]
  50. Romagnesi H. 1967. Les russules d’Europe et d’Afrique du Nord [The Russula of Europe and North Africa]. Paris: Bordas. [Google Scholar]
  51. Romagnesi H. 1985. Les russules d’Europe et d’Afrique du Nord [The Russula of Europe and North Africa]. Lehre: Vaduz. [Google Scholar]
  52. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP.. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic. 61:539–542. doi: 10.1093/sysbio/sys029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Sarnari M. 1998. Monografia illustrata del genere Russula in Europa [Illustrated monograph of the genus Russula in Europe]. Trento: Fondazione centro studi micologici. [Google Scholar]
  54. Sarnari M, Redeuilh G. 2005. Monografia illustrata del genere Russula in europa [illustrated monograph of the genus Russula in Europe]. Trento: Associazione Micologica Bresadola. [Google Scholar]
  55. Sarwar S, Aziz T, Hanif M, Ilyas S, Saba M, Khalid S, Fiaz M. 2020. Plectological and molecular identification of economically important wild Russulales mushrooms from Pakistan and their antifungal potential against food pathogenic fungus Aspergillus niger. Bangl J Plant Taxon. 27(1):67–77. doi: 10.3329/bjpt.v27i1.47568. [DOI] [Google Scholar]
  56. Silvestro D, Michalak I.. 2012. raxmlGUI: a graphical front-end for RAxML. Org Divers Evol. 12:335–337. doi: 10.1007/s13127-011-0056-0. [DOI] [Google Scholar]
  57. Singer R. 1968. Les Russules d’Europe et d’Afrique du Nord [Russula of Europe and North Africa]. Paris: Jstor. [Google Scholar]
  58. Song Y, Xie XC, Buyck B. 2021. Two novel species of subgenus Russula crown clade (Russulales, Basidiomycota) from China. Mus Natl Hist Nat. 775:15–33. doi: 10.5852/ejt.2021.775.1543. [DOI] [Google Scholar]
  59. White T, Bruns T, Lee S, Taylor F, White T, Lee SH, Taylor L, Shawetaylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. Mycologia. 18(1):315–322. [Google Scholar]
  60. Zhang D, Gao F, Jakovli I, Zou H, Wang GT. 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 20(1):348–355. doi: 10.1111/1755-0998.13096. [DOI] [PubMed] [Google Scholar]
  61. Zhou H, Cheng GQ, Wang QT, Guo MJ, Zhuo L, Yan HF, Li GJ, Hou CL. 2022. Morphological characteristics and phylogeny reveal six new species in Russula Subgenus Russula (Russulaceae, Russulales) from Yanshan Mountains, North China. J Fungi. 8(12):1283. doi: 10.3390/jof8121283. [DOI] [PMC free article] [PubMed] [Google Scholar]

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